Rate thresholds determine the precision of temporal integration in principal cells of the ventral cochlear nucleus

Hearing Research

Volumn 216-217, Issue 1-2, 2006, Pages 52-63

  McGinley, Matthew J ^a   Oertel, Donata ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Action potential generation; Current ramp; Integration window; Synaptic integration; Temporal coding; Temporal summation; Ventral cochlear nucleus

Indexed keywords

ALPHA DENDROTOXIN; DENDROTOXIN; UNCLASSIFIED DRUG;

ACCURACY; ANIMAL TISSUE; ARTICLE; AUDITORY THRESHOLD; CELL TYPE; COCHLEAR NUCLEUS; CONTROLLED STUDY; DEPOLARIZATION; MOUSE; NERVE CELL; NERVE POTENTIAL; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; STELLATE CELL; SYNAPTIC POTENTIAL; TEMPORAL SUMMATION;

ACTION POTENTIALS; ANIMALS; COCHLEAR NUCLEUS; EXCITATORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED ICR; NEURONS; PATCH-CLAMP TECHNIQUES; SYNAPSES; TIME FACTORS;

EID: 33745005512     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2006.02.006     Document Type: Article

References (93)

1. Adams J.C. Projections from octopus cells of the posteroventral cochlear nucleus to the ventral nucleus of the lateral lemniscus in cat and human. Aud. Neurosci. 3 (1997) 335-350
2. Adams J.C., and Warr W.B. Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J. Comp. Neurol. 170 (1976) 107-121
3. Azouz R., and Gray C.M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc. Natl. Acad. Sci. USA 97 (2000) 8110-8115
4. Azouz R., and Gray C.M. Adaptive coincidence detection and dynamic gain control in visual cortical neurons in vivo. Neuron 37 (2003) 513-523
5. Bair W., and Movshon J.A. Adaptive temporal integration of motion in direction-selective neurons in macaque visual cortex. J. Neurosci. 24 (2004) 7305-7323
6. Bal R., and Oertel D. Hyperpolarization-activated, mixed-cation current (Ih) in octopus cells of the mammalian cochlear nucleus. J. Neurophysiol. 84 (2000) 806-817
7. Bal R., and Oertel D. Potassium currents in octopus cells of the mammalian cochlear nuclei. J. Neurophysiol. 86 (2001) 2299-2311
8. Barnes-Davies M., Barker M.C., Osmani F., and Forsythe I.D. Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur. J. Neurosci. 19 (2004) 325-333
9. Blackburn C.C., and Sachs M.B. Classification of unit types in the anteroventral cochlear nucleus: PST histograms and regularity analysis. J. Neurophysiol. 62 (1989) 1303-1329
10. Brawer J.R., Morest D.K., and Kane E.C. The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol. 155 (1974) 251-300
11. Brew H.M., and Forsythe I.D. Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse. J. Neurosci. 15 (1995) 8011-8022
12. Brew H.M., and Forsythe I.D. Systematic variation of potassium current amplitudes across the tonotopic axis of the rat medial nucleus of the trapezoid body. Hear. Res. 206 (2005) 116-132
13. Brew H.M., Hallows J.L., and Tempel B.L. Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1. J. Physiol. 548 (2003) 1-20
14. Cant N.B. Identification of cell types in the anteroventral cochlear nucleus that project to the inferior colliculus. Neurosci. Lett. 32 (1982) 241-246
15. Cant N.B., and Casseday J.H. Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J. Comp. Neurol. 247 (1986) 457-476
16. Cao X., and Oertel D. Temperature affects voltage-sensitive conductances differentially in octopus cells of the mammalian cochlear nucleus. J. Neurophysiol. 94 (2005) 821-832
17. Cao X., and Oertel D. Voltage-sensitive conductances in bushy cells of the ventral cochlear nucleus of mice. Ass. Res. Otolargyngol. Abstr. (2006) 29
18. Carney L.H. Temporal response properties of neurons in the auditory pathway. Curr. Opin. Neurobiol. 9 (1999) 442-446
19. Carney L.H., and Friedman M. Spatiotemporal tuning of low-frequency cells in the anteroventral cochlear nucleus. J. Neurosci. 18 (1998) 1096-1104
20. Dodson P.D., Barker M.C., and Forsythe I.D. Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J. Neurosci. 22 (2002) 6953-6961
21. Doucet J.R., and Ryugo D.K. Projections from the ventral cochlear nucleus to the dorsal cochlear nucleus in rats. J. Comp. Neurol. 385 (1997) 245-264
22. Ferragamo M.J., and Oertel D. Octopus cells of the mammalian ventral cochlear nucleus sense the rate of depolarization. J. Neurophysiol. 87 (2002) 2262-2270
23. Ferragamo M.J., Golding N.L., and Oertel D. Synaptic inputs to stellate cells in the ventral cochlear nucleus. J. Neurophysiol. 79 (1998) 51-63
24. Forsythe I.D., and Barnes-Davies M. The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc. Roy. Soc. Lond. - Series B: Biol. Sci. 251 (1993) 143-150
25. Fujino K., and Oertel D. Cholinergic modulation of stellate cells in the mammalian ventral cochlear nucleus. J. Neurosci. 21 (2001) 7372-7383
26. Gardner S.M., Trussell L.O., and Oertel D. Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input. J. Neurosci. 19 (1999) 8721-8729
27. Glendenning K.K., Brunso-Bechtold J.K., Thompson G.C., and Masterton R.B. Ascending auditory afferents to the nuclei of the lateral lemniscus. J. Comp. Neurol. 197 (1981) 673-703
28. Godfrey D.A., Kiang N.Y.S., and Norris B.E. Single unit activity in the posteroventral cochlear nucleus of the cat. J. Comp. Neurol. 162 (1975) 247-268
29. Golding N.L., Robertson D., and Oertel D. Recordings from slices indicate that Octopus cells of the cochlear nucleus detect coincident firing of auditory nerve fibers with temporal precision. J. Neurosci. 15 (1995) 3138-3153
30. Golding N.L., Ferragamo M.J., and Oertel D. Role of intrinsic conductances underlying responses to transients in Octopus cells of the cochlear nucleus. J. Neurosci. 19 (1999) 2897-2905
31. Grissmer S., Nguyen A.N., Aiyar J., Hanson D.C., Mather R.J., Gutman G.A., Karmilowicz M.J., Auperin D.D., and Chandy K.G. Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45 (1994) 1227-1234
32. Hopkins W.F. Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther. 285 (1998) 1051-1060
33. Hopkins W.F., Allen M.L., Houamed K.M., and Tempel B.L. Properties of voltage-gated K+ currents expressed in Xenopus oocytes by mKv1.1, mKv1.2 and their heteromultimers as revealed by mutagenesis of the dendrotoxin-binding site in mKv1.1. Eur. J. Physiol. 428 (1994) 382-390
34. Joris P.X., Carney L.H., Smith P.H., and Yin T.C. Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J. Neurophysiol. 71 (1994) 1022-1036
35. Joris P.X., Smith P.H., and Yin T.C. Enhancement of neural synchronization in the anteroventral cochlear nucleus. II. Responses in the tuning curve tail. J. Neurophysiol. 71 (1994) 1037-1051
36. Koch C., Rapp M., and Segev I. A brief history of time (constants). Cereb. Cortex 6 (1996) 93-101
37. Kopp-Scheinpflug C., Fuchs K., Lippe W.R., Tempel B.L., and Rubsamen R. Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J. Neurosci. 23 (2003) 9199-9207
38. Liberman M.C. Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J. Comp. Neurol. 313 (1991) 240-258
39. Liberman M.C. Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J. Comp. Neurol. 313 (1991) 240-258
40. Magee J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18 (1998) 7613-7624
41. Mainen Z.F., Joerges J., Huguenard J.R., and Sejnowski T.J. A model of spike initiation in neocortical pyramidal neurons. Neuron 15 (1995) 1427-1439
42. Manis P.B., and Marx S.O. Outward currents in isolated ventral cochlear nucleus neurons. J. Neurosci. 11 (1991) 2865-2880
43. McGinley M.J., Lazimy Y.M., Bal R., and Oertel D. Measurement and modeling of cable properties and optimal input delay profiles in Octopus cells of the ventral cochlear nucleus. Ass. Res. Otolargyngol. Abstr. (2005) 28
44. McGinley M.J., Rodrigues A.R.A., and Oertel D. Integration window for detection of inputs in neurons of the ventral cochlear nucleus. Ass. Res. Otolaryngol. Abstr. (2005) 28
45. Migliore M. On the integration of subthreshold inputs from Perforant Path and Schaffer Collaterals in hippocampal CA1 pyramidal neurons. J. Comput. Neurosci. 14 (2003) 185-192
46. Mittmann W., Koch U., and Hausser M. Feed-forward inhibition shapes the spike output of cerebellar Purkinje cells. J. Physiol. 563 (2005) 369-378
47. Møller A.R. Unit responses in the rat cochlear nucleus to repetitive, transient sounds. Acta Physiol. Scand. 75 (1969) 542-551
48. Møller A.R. Unit responses in the rat cochlear nucleus to tones of rapidly varying frequency and amplitude. Acta Physiol. Scand. 81 (1971) 540-556
49. Møller A.R. Coding of sounds with rapidly varying spectrum in the cochlear nucleus. J. Acoust. Soc. Am. 55 (1974) 631-640
50. Møller A.R. Latency of unit responses in cochlear nucleus determined in two different ways. J. Neurophysiol. 38 (1975) 812-821
51. Møller A.R. Dynamic properties of primary auditory fibers compared with cells in the cochlear nucleus. Acta Physiol. Scand. 98 (1976) 157-167
52. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J. Neurosci. 3 (1983) 2043-2053
53. Oertel D. Use of brain slices in the study of the auditory system: spatial and temporal summation of synaptic inputs in cells in the anteroventral cochlear nucleus of the mouse. J. Acous. Soc. Am. 78 (1985) 328-333
54. Oertel D., Wu S.H., Garb M.W., and Dizack C. Morphology and physiology of cells in slice preparations of the posteroventral cochlear nucleus of mice. J. Comp. Neurol. 295 (1990) 136-154
55. Oertel D., Bal R., Gardner S.M., Smith P.H., and Joris P.X. Detection of synchrony in the activity of auditory nerve fibers by Octopus cells of the mammalian cochlear nucleus. Proc. Natl. Acad. Sci. USA 97 (2000) 11773-11779
56. Oleskevich S., and Walmsley B. Synaptic transmission in the auditory brainstem of normal and congenitally deaf mice. J. Physiol. 540 (2002) 447-455
57. Osen K.K. Cytoarchitecture of the cochlear nuclei in the cat. J. Comp. Neurol. 136 (1969) 453-484
58. Owen D.G., Hall A., Stephens G., Stow J., and Robertson B. The relative potencies of dendrotoxins as blockers of the cloned voltage-gated K+ channel, mKv1.1 (MK-1), when stably expressed in Chinese hamster ovary cells. Br. J. Pharmacol. 120 (1997) 1029-1034
59. Pfeiffer R.R. Anteroventral cochlear nucleus: wave forms of extracellularly recorded spike potentials. Science 154 (1966) 667-668
60. Pouille F., and Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293 (2001) 1159-1163
61. Price G.R. Action potentials in the cat at low sound intensities: thresholds, latencies, and rates of change. J. Acous. Soc. Am. 64 (1978) 1400-1405
62. Rathouz M., and Trussell L. Characterization of outward currents in neurons of the avian nucleus magnocellularis. J. Neurophysiol. 80 (1998) 2824-2835
63. Rhode W.S., and Smith P.H. Encoding timing and intensity in the ventral cochlear nucleus of the cat. J. Neurophysiol. 56 (1986) 261-286
64. Rhode W.S., Oertel D., and Smith P.H. Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat ventral cochlear nucleus. J. Comp. Neurol. 213 (1983) 448-463
65. Rodrigues A.R.A., and Oertel D. Hyperpolarization-activated currents regulate excitability in stellate cells of the mammalian ventral cochlear nucleus. J. Neurophysiol. 95 (2006) 76-87
66. Rothman J.S., and Manis P.B. Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons. J. Neurophysiol. 89 (2003) 3083-3096
67. Rothman J.S., and Manis P.B. The roles potassium currents play in regulating the electrical activity of ventral cochlear nucleus neurons. J. Neurophysiol. 89 (2003) 3097-3113
68. Schofield B.R. Projections from the cochlear nucleus to the superior paraolivary nucleus in guinea pigs. J. Comp. Neurol. 360 (1995) 135-149
69. Schofield B.R., and Cant N.B. Ventral nucleus of the lateral lemniscus in guinea pigs: cytoarchitecture and inputs from the cochlear nucleus. J. Comp. Neurol. 379 (1997) 363-385
70. Schwarz D.W., and Puil E. Firing properties of spherical bushy cells in the anteroventral cochlear nucleus of the gerbil. Hear. Res. 114 (1997) 127-138
71. Scott L.L., Mathews P.J., and Golding N.L. Posthearing developmental refinement of temporal processing in principal neurons of the medial superior olive. J. Neurosci. 25 (2005) 7887-7895
72. Sekerli M., Del Negro C.A., Lee R.H., and Butera R.J. Estimating action potential thresholds from neuronal time-series: new metrics and evaluation of methodologies. IEEE Trans. Biomed. Eng. 51 (2004) 1665-1672
73. Smith P.H., and Rhode W.S. Characterization of HRP-labeled globular bushy cells in the cat anteroventral cochlear nucleus. J. Comp. Neurol. 266 (1987) 360-375
74. Smith P.H., and Rhode W.S. Structural and functional properties distinguish two types of multipolar cells in the ventral cochlear nucleus. J. Comp. Neurol. 282 (1989) 595-616
75. Smith P.H., Joris P.X., Banks M.I., and Yin T.C.T. Responses of cochlear nucleus cells and projections of their axons. In: Merchan M.A., Juiz J.M., Godfrey D.A., and Mugnaini E. (Eds). The Mammalian Cochlear Nuclei, Organization and Function (1993), Plenum Press, New York and London 349-360
76. Smith P.H., Massie A., and Joris P.X. Acoustic stria: anatomy of physiologically characterized cells and their axonal projection patterns. J. Comp. Neurol. 482 (2005) 349-371
77. Soares D., Chitwood R.A., Hyson R.L., and Carr C.E. Intrinsic neuronal properties of the chick nucleus angularis. J. Neurophysiol. 88 (2002) 152-162
78. Song P., Yang Y., Barnes-Davies M., Bhattacharjee A., Hamann M., Forsythe I.D., Oliver D.L., and Kaczmarek L.K. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat. Neurosci. 10 (2005) 1335-1342
79. Spirou, G.A., Rager, J., Manis, P.B., 2005 Convergence of auditory nerve fiber projections onto globular bushy cells. Soc. Neurosci. Abstr., Program No. 44.7.
80. Svirskis G., and Rinzel J. Influence of subthreshold nonlinearities on signal-to-noise ratio and timing precision for small signals in neurons: minimal model analysis. Network 14 (2003) 137-150
81. Svirskis G., Dodla R., and Rinzel J. Subthreshold outward currents enhance temporal integration in auditory neurons. Biol. Cybern. 89 (2003) 333-340
82. Svirskis G., Kotak V., Sanes D.H., and Rinzel J. Sodium along with low-threshold potassium currents enhance coincidence detection of subthreshold noisy signals in MSO neurons. J. Neurophysiol. 91 (2004) 2465-2473
83. Tolbert L.P., Morest D.K., and Yurgelun-Todd D.A. The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: horseradish peroxidase labelling of identified cell types. Neuroscience 7 (1982) 3031-3052
84. Trussell L.O. Cellular mechanisms for preservation of timing in central auditory pathways. Curr. Opin. Neurobiol. 7 (1997) 487-492 (Review, 49 refs)
85. Wang H., Kunkel D.D., Schwartzkroin P.A., and Tempel B.L. Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J. Neurosci. 14 (1994) 4588-4599
86. Wang F.C., Parcej D.N., and Dolly J.O. alpha subunit compositions of Kv1.1-containing K+ channel subtypes fractionated from rat brain using dendrotoxins. Eur. J. Biochem. 263 (1999) 230-237
87. White J.A., Young E.D., and Manis P.B. The electrotonic structure of regular-spiking neurons in the ventral cochlear nucleus may determine their response properties. J. Neurophysiol. 71 (1994) 1774-1786
88. Winter I.M., and Palmer A.R. Temporal responses of primary like anteroventral cochlear nucleus units to the steady-state vowel /i/. J. Acoust. Soc. Am. 88 (1990) 1437-1441
89. Wu S.H., and Kelly J.B. In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. I. Membrane and synaptic response properties. J. Neurophysiol. 73 (1995) 780-793
90. Wu S.H., and Oertel D. Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J. Neurosci. 4 (1984) 1577-1588
91. Wu S.H., and Oertel D. Maturation of synapses and electrical properties. Hear. Res. 30 (1987) 99-110
92. Zhang X., and Carney L.H. Response properties of an integrate-and-fire model that receives subthreshold inputs. Neural Comput. 17 (2005) 2571-2601
93. Zhao M., and Wu S.H. Morphology and physiology of neurons in the ventral nucleus of the lateral lemniscus in rat brain slices. J. Comp. Neurol. 433 (2001) 255-271